In utero hematopoietic cell transplantation - Recent progress and the potential for clinical application

Cytotherapy

Volumn 15, Issue 5, 2013, Pages 525-535

  Vrecenak, Jesse D ^a   Flake, Alan W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

fetal therapy; hematopoietic stem cell transplantation; in utero; tolerance

Indexed keywords

CELL HOMING; CHEDIAK HIGASHI SYNDROME; CHIMERA; CHRONIC GRANULOMATOUS DISEASE; DIZYGOTIC TWINS; ENGRAFTMENT; GESTATION PERIOD; GRAFT VERSUS HOST REACTION; HEMATOPOIESIS; HEMATOPOIETIC CELL; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENCE; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; IN UTERO STEM CELL TRANSPLANTATION; LYMPHOCYTE SUBPOPULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROCHIMERISM; MONONUCLEAR CELL; MYELOABLATIVE CONDITIONING; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; REVIEW; X LINKED SEVERE COMBINED IMMUNODEFICIENCY;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; DISEASE MODELS, ANIMAL; HEMATOLOGIC DISEASES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNE TOLERANCE; TRANSPLANTATION CHIMERA;

EID: 84875699969     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2013.01.003     Document Type: Review

References (109)

1. R.E. Billingham, L. Brent, and P.B. Medawar Actively acquired tolerance of foreign cells Nature 172 1953 603 606
2. A.D. Griesemer, E.C. Sorenson, and M.A. Hardy The role of the thymus in tolerance Transplantation 90 2010 465 474
3. E. Palmer Negative selection: clearing out the bad apples from the T-cell repertoire Nat Rev Immunol 3 2003 383 391
4. F. Ramsdell, and B.J. Fowlkes Clonal deletion versus clonal anergy: the role of the thymus in inducing self tolerance Science 248 1990 1342 1348
5. C.C. Goodnow, J. Sprent, B. Fazekas de St Groth, and C.G. Vinuesa Cellular and genetic mechanisms of self tolerance and autoimmunity Nature 435 2005 590 597
6. A.M. Gallegos, and M.J. Bevan Central tolerance: good but imperfect Immunol Rev 209 2006 290 296
7. I.A. Parish, and W.R. Heath Too dangerous to ignore: self-tolerance and the control of ignorant autoreactive T cells Immunol Cell Biol 86 2008 146 152
8. S.Z. Josefowicz, L.F. Lu, and A.Y. Rudensky Regulatory T cells: mechanisms of differentiation and function Annu Rev Immunol 30 2012 531 564
9. T. Takahashi, T. Tagami, S. Yamazaki, T. Uede, J. Shimizu, and N. Sakaguchi Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4 J Exp Med 192 2000 303 310
10. D.J. Merianos, E. Tiblad, M.T. Santore, C.A. Todorow, P. Laje, and M. Endo Maternal alloantibodies induce a postnatal immune response that limits engraftment following in utero hematopoietic cell transplantation in mice J Clin Invest 119 2009 2590 2600
11. J. Leventhal, Y. Huang, H. Xu, I. Goode, and S.T. Ildstad Novel regulatory therapies for prevention of Graft-versus-host disease BMC Med 10 2012 48
12. H.K. Mikkola, C. Gekas, S.H. Orkin, and F. Dieterlen-Lievre Placenta as a site for hematopoietic stem cell development Exp Hematol 33 2005 1048 1054
13. J.L. Christensen, D.E. Wright, A.J. Wagers, and I.L. Weissman Circulation and chemotaxis of fetal hematopoietic stem cells PLoS Biol 2 2004 E75
14. M. Tavian, and B. Peault Embryonic development of the human hematopoietic system Int J Dev Biol 49 2005 243 250
15. A.T. Badillo, and A.W. Flake The regulatory role of stromal microenvironments in fetal hematopoietic ontogeny Stem Cell Rev 2 2006 241 246
16. R.D. Owen Immunogenetic consequences of vascular anastomoses between bovine twins Science 102 1945 400 401
17. F.M. Burnet, and F. Fenner The Production of Antibodies 1949 MacMillan London
18. D. Anderson, R. Billingham, G. Lampkin, and P. Medawar The use of skin grafting to distinguish between monozygotic and dizygotic twins in cattle Heredity 5 1951 379 397
19. J.F. Crow A golden anniversary: cattle twins and immune tolerance Genetics 144 1996 855 859
20. R. Cragle, and W.H. Stone Preliminary results of kidney grafts between cattle chimeric twins Transplantation 5 1967 328 335
21. J. Picus, W.R. Aldrich, and N.L. Letvin A naturally occurring bone marrow-chimeric primate, I: integrity of its immune system Transplantation 39 1985 297 303
22. J. Picus, K. Holley, W.R. Aldrich, J.D. Griffin, and N.L. Letvin A naturally occurring bone marrow-chimeric primate, II: environment dictates restriction on cytolytic T lymphocyte-target cell interactions J Exp Med 162 1985 2035 2052
23. T.J. Gill 3rd Chimerism in humans Transplant Proc 9 1977 1423 1431
24. B.A. van Dijk, D.I. Boomsma, and A.J. de Man Blood group chimerism in human multiple births is not rare Am J Med Genet 61 1996 264 268
25. H.E. Hansen, E. Niebuhr, and C. Lomas Chimeric twins: T.S. and M.R. reexamined Hum Hered 34 1984 127 130
26. R.A. Fleischman, and B. Mintz Prevention of genetic anemias in mice by microinjection of normal hematopoietic stem cells into the fetal placenta Proc Natl Acad Sci U S A 76 1979 5736 5740
27. B. Mintz, K. Anthony, and S. Litwin Monoclonal derivation of mouse myeloid and lymphoid lineages from totipotent hematopoietic stem cells experimentally engrafted in fetal hosts Proc Natl Acad Sci U S A 81 1984 7835 7839
28. B.R. Blazar, P.A. Taylor, and D.A. Vallera In utero transfer of adult bone marrow cells into recipients with severe combined immunodeficiency disorder yields lymphoid progeny with T- and B-cell functional capabilities Blood 86 1995 4353 4366
29. B.R. Blazar, P.A. Taylor, and D.A. Vallera Adult bone marrow-derived pluripotent hematopoietic stem cells are engraftable when transferred in utero into moderately anemic fetal recipients Blood 85 1995 833 841
30. D.R. Archer, C.W. Turner, A.M. Yeager, and W.H. Fleming Sustained multilineage engraftment of allogeneic hematopoietic stem cells in NOD/SCID mice after in utero transplantation Blood 90 1997 3222 3229
31. E. Carrier, T.H. Lee, M.P. Busch, and M.J. Cowan Induction of tolerance in nondefective mice after in utero transplantation of major histocompatibility complex-mismatched fetal hematopoietic stem cells Blood 86 1995 4681 4690
32. J. Donahue, E. Gilpin, T.H. Lee, M.P. Busch, M. Croft, and E. Carrier Microchimerism does not induce tolerance and sustains immunity after in utero transplantation Transplantation 71 2001 359 368
33. H.B. Kim, A.F. Shaaban, E.Y. Yang, K.W. Liechty, and A.W. Flake Microchimerism and tolerance after in utero bone marrow transplantation in mice J Surg Res 77 1998 1 5
34. K.L. Lovell, S.A. Kraemer, J.R. Leipprandt, D.J. Sprecher, N.K. Ames, and J. Nichols-Torrez In utero hematopoietic stem cell transplantation: a caprine model for prenatal therapy in inherited metabolic diseases Fetal Diagn Ther 16 2001 13 17
35. R.D. Pearce, D. Kiehm, D.T. Armstrong, P.B. Little, J.W. Callahan, and L.R. Klunder Induction of hemopoietic chimerism in the caprine fetus by intraperitoneal injection of fetal liver cells Experientia 45 1989 307 308
36. K. Blakemore, C. Hattenburg, G. Stetten, K. Berg, S. South, and K. Murphy In utero hematopoietic stem cell transplantation with haploidentical donor adult bone marrow in a canine model Am J Obstet Gynecol 190 2004 960 973
37. W.H. Peranteau, T.E. Heaton, Y.C. Gu, S.W. Volk, T.R. Bauer, and K. Alcorn Haploidentical in utero hematopoietic cell transplantation improves phenotype and can induce tolerance for postnatal same-donor transplants in the canine leukocyte adhesion deficiency model Biol Blood Marrow Transplant 15 2009 293 305
38. M.R. Harrison, R.N. Slotnick, T.M. Crombleholme, M.S. Golbus, A.F. Tarantal, and E.D. Zanjani In-utero transplantation of fetal liver haemopoietic stem cells in monkeys Lancet 2 1989 1425 1427
39. M.J. Cowan, A.F. Tarantal, J. Capper, M. Harrison, and M. Garovoy Long-term engraftment following in utero T cell-depleted parental marrow transplantation into fetal rhesus monkeys Bone Marrow Transplant 17 1996 1157 1165
40. L.E. Shields, L.K. Gaur, M. Gough, J. Potter, A. Sieverkropp, and R.G. Andrews In utero hematopoietic stem cell transplantation in nonhuman primates: the role of T cells Stem Cells 21 2003 304 314
41. A.W. Flake, M.R. Harrison, N.S. Adzick, and E.D. Zanjani Transplantation of fetal hematopoietic stem cells in utero: the creation of hematopoietic chimeras Science 233 1986 776 778
42. E.D. Zanjani, M.G. Pallavicini, J.L. Ascensao, A.W. Flake, R.G. Langlois, and M. Reitsma Engraftment and long-term expression of human fetal hemopoietic stem cells in sheep following transplantation in utero J Clin Invest 89 1992 1178 1188
43. E.F. Srour, E.D. Zanjani, J.E. Brandt, T. Leemhuis, R.A. Briddell, and N.A. Heerema Sustained human hematopoiesis in sheep transplanted in utero during early gestation with fractionated adult human bone marrow cells Blood 79 1992 1404 1412
44. E.D. Zanjani, A.W. Flake, H. Rice, M. Hedrick, and M. Tavassoli Long-term repopulating ability of xenogeneic transplanted human fetal liver hematopoietic stem cells in sheep J Clin Invest 93 1994 1051 1055
45. H.B. Kim, A.F. Shaaban, R. Milner, C. Fichter, and A.W. Flake In utero bone marrow transplantation induces donor-specific tolerance by a combination of clonal deletion and clonal anergy J Pediatr Surg 34 1999 726 730
46. E.H. Javazon, A.M. Merchant, E. Danzer, and A.W. Flake Reconstitution of hematopoiesis following intrauterine transplantation of stem cells Methods Mol Med 105 2005 81 94
47. S. Hayashi, M. Hsieh, W.H. Peranteau, S. Ashizuka, and A.W. Flake Complete allogeneic hematopoietic chimerism achieved by in utero hematopoietic cell transplantation and cotransplantation of LLME-treated, MHC-sensitized donor lymphocytes Exp Hematol 32 2004 290 299
48. S. Hayashi, O. Abdulmalik, W.H. Peranteau, S. Ashizuka, C. Campagnoli, and Q. Chen Mixed chimerism following in utero hematopoietic stem cell transplantation in murine models of hemoglobinopathy Exp Hematol 31 2003 176 184
49. W.H. Peranteau, M. Endo, O.O. Adibe, A. Merchant, P.W. Zoltick, and A.W. Flake CD26 inhibition enhances allogeneic donor-cell homing and engraftment after in utero hematopoietic-cell transplantation Blood 108 2006 4268 4274
50. P.W. Lee, R.A. Cina, M.A. Randolph, J. Goodrich, H. Rowland, and R. Arellano Stable multilineage chimerism across full MHC barriers without graft-versus-host disease following in utero bone marrow transplantation in pigs Exp Hematol 33 2005 371 379
51. P.W. Lee, R.A. Cina, M.A. Randolph, R. Arellano, J. Goodrich, and H. Rowland In utero bone marrow transplantation induces kidney allograft tolerance across a full major histocompatibility complex barrier in Swine Transplantation 79 2005 1084 1090
52. W.H. Peranteau, S. Hayashi, M. Hsieh, A.F. Shaaban, and A.W. Flake High-level allogeneic chimerism achieved by prenatal tolerance induction and postnatal nonmyeloablative bone marrow transplantation Blood 100 2002 2225 2234
53. A.W. Flake, and E.D. Zanjani In utero hematopoietic stem cell transplantation: ontogenic opportunities and biologic barriers Blood 94 1999 2179 2191
54. A.F. Shaaban, H.B. Kim, R. Milner, and A.W. Flake A kinetic model for the homing and migration of prenatally transplanted marrow Blood 94 1999 3251 3257
55. N.S. Wolf, I. Bertoncello, D. Jiang, and G. Priestley Developmental hematopoiesis from prenatal to young-adult life in the mouse model Exp Hematol 23 1995 142 146
56. D.E. Harrison, and C.M. Astle Short- and long-term multilineage repopulating hematopoietic stem cells in late fetal and newborn mice: models for human umbilical cord blood Blood 90 1997 174 181
57. S.S. Rao, S.O. Peters, R.B. Crittenden, F.M. Stewart, H.S. Ramshaw, and P.J. Quesenberry Stem cell transplantation in the normal nonmyeloablated host: relationship between cell dose, schedule, and engraftment Exp Hematol 25 1997 114 121
58. F.M. Stewart, R.B. Crittenden, P.A. Lowry, S. Pearson-White, and P.J. Quesenberry Long-term engraftment of normal and post-5-fluorouracil murine marrow into normal nonmyeloablated mice Blood 81 1993 2566 2571
59. H.S. Ramshaw, R.B. Crittenden, M. Dooner, S.O. Peters, S.S. Rao, and P.J. Quesenberry High levels of engraftment with a single infusion of bone marrow cells into normal unprepared mice Biol Blood Marrow Transplant 1 1995 74 80
60. W.H. Peranteau, M. Endo, O.O. Adibe, and A.W. Flake Evidence for an immune barrier after in utero hematopoietic-cell transplantation Blood 109 2007 1331 1333
61. D.E. Harrison, R.K. Zhong, C.T. Jordan, I.R. Lemischka, and C.M. Astle Relative to adult marrow, fetal liver repopulates nearly five times more effectively long-term than short-term Exp Hematol 25 1997 293 297
62. C.T. Jordan, C.M. Astle, J. Zawadzki, K. Mackarehtschian, I.R. Lemischka, and D.E. Harrison Long-term repopulating abilities of enriched fetal liver stem cells measured by competitive repopulation Exp Hematol 23 1995 1011 1015
63. W. Leung, M. Ramirez, and C.I. Civin Quantity and quality of engrafting cells in cord blood and autologous mobilized peripheral blood Biol Blood Marrow Transplant 5 1999 69 76
64. E.S. Rosler, J.E. Brandt, J. Chute, and R. Hoffman An in vivo competitive repopulation assay for various sources of human hematopoietic stem cells Blood 96 2000 3414 3421
65. K. Howson-Jan, Y.H. Matloub, D.A. Vallera, and B.R. Blazar In utero engraftment of fully H-2-incompatible versus congenic adult bone marrow transferred into nonanemic or anemic murine fetal recipients Transplantation 56 1993 709 716
66. R.A. Fleischman, and B. Mintz Development of adult bone marrow stem cells in H-2-compatible and -incompatible mouse fetuses J Exp Med 159 1984 731 745
67. A.W. Flake, M.G. Roncarolo, J.M. Puck, G. Almeida-Porada, M.I. Evans, and M.P. Johnson Treatment of X-linked severe combined immunodeficiency by in utero transplantation of paternal bone marrow N Engl J Med 335 1996 1806 1810
68. J.L. Touraine, D. Raudrant, C. Royo, A. Rebaud, M.G. Roncarolo, and G. Souillet In-utero transplantation of stem cells in bare lymphocyte syndrome Lancet 1 1989 1382
69. M. Westgren, O. Ringden, P. Bartmann, T.H. Bui, B. Lindton, and J. Mattsson Prenatal T-cell reconstitution after in utero transplantation with fetal liver cells in a patient with X-linked severe combined immunodeficiency Am J Obstet Gynecol 187 2002 475 482
70. M.C. Renda, E. Fecarotta, F. Dieli, L. Markling, M. Westgren, and G. Damiani Evidence of alloreactive T lymphocytes in fetal liver: implications for fetal hematopoietic stem cell transplantation Bone Marrow Transplant 25 2000 135 141
71. P. Toivanen, J. Uksila, A. Leino, O. Lassila, T. Hirvonen, and O. Ruuskanen Development of mitogen responding T cells and natural killer cells in the human fetus Immunol Rev 57 1981 89 105
72. M. Blackman, J. Kappler, and P. Marrack The role of the T cell receptor in positive and negative selection of developing T cells Science 248 1990 1335 1341
73. R.H. Schwartz Acquisition of immunologic self-tolerance Cell 57 1989 1073 1081
74. W.C. Sha, C.A. Nelson, R.D. Newberry, D.M. Kranz, J.H. Russell, and D.Y. Loh Positive and negative selection of an antigen receptor on T-cells in transgenic mice Nature 336 1988 73 76
75. S. Hayashi, W.H. Peranteau, A.F. Shaaban, and A.W. Flake Complete allogeneic hematopoietic chimerism achieved by a combined strategy of in utero hematopoietic stem cell transplantation and postnatal donor lymphocyte infusion Blood 100 2002 804 812
76. A. Nijagal, M. Wegorzewska, E. Jarvis, T. Le, Q. Tang, and T.C. MacKenzie Maternal T cells limit engraftment after in utero hematopoietic cell transplantation in mice J Clin Invest 121 2011 582 592
77. M.C. Yoder, J.G. Cumming, K. Hiatt, P. Mukherjee, and D.A. Williams A novel method of myeloablation to enhance engraftment of adult bone marrow cells in newborn mice Biol Blood Marrow Transplant 2 1996 59 67
78. T. Abe, S. Masuda, Y. Tanaka, S. Nitta, Y. Kitano, and S. Hayashi Maternal administration of busulfan before in utero transplantation of human hematopoietic stem cells enhances engraftments in sheep Exp Hematol 40 2012 436 444
79. K.W. Christopherson 2nd, G. Hangoc, and H.E. Broxmeyer Cell surface peptidase CD26/dipeptidylpeptidase IV regulates CXCL12/stromal cell-derived factor-1 alpha-mediated chemotaxis of human cord blood CD34+ progenitor cells J Immunol 169 2002 7000 7008
80. G. Almeida-Porada, A.W. Flake, H.A. Glimp, and E.D. Zanjani Cotransplantation of stroma results in enhancement of engraftment and early expression of donor hematopoietic stem cells in utero Exp Hematol 27 1999 1569 1575
81. G. Almeida-Porada, C.D. Porada, N. Tran, and E.D. Zanjani Cotransplantation of human stromal cell progenitors into preimmune fetal sheep results in early appearance of human donor cells in circulation and boosts cell levels in bone marrow at later time points after transplantation Blood 95 2000 3620 3627
82. Y. Huang, L.D. Bozulic, T. Miller, H. Xu, L.R. Hussain, and S.T. Ildstad CD8α+ plasmacytoid precursor DCs induce antigen-specific regulatory T cells that enhance HSC engraftment in vivo Blood 117 2011 2494 2505
83. A.F. Shaaban, H.B. Kim, L. Gaur, K.W. Liechty, and A.W. Flake Prenatal transplantation of cytokine-stimulated marrow improves early chimerism in a resistant strain combination but results in poor long-term engraftment Exp Hematol 34 2006 1278 1287
84. T.M. Crombleholme, M.R. Harrison, and E.D. Zanjani In utero transplantation of hematopoietic stem cells in sheep: the role of T cells in engraftment and graft-versus-host disease J Pediatr Surg 25 1990 885 892
85. S.M. Petersen, M. Gendelman, K.M. Murphy, M. Torbenson, R.J. Jones, and J.E. Althaus Use of T-cell antibodies for donor dosaging in a canine model of in utero hematopoietic stem cell transplantation Fetal Diagn Ther 22 2007 175 179
86. S. Bhattacharyya, A. Chawla, K. Smith, Y. Zhou, S. Talib, and B. Wardwell Multilineage engraftment with minimal graft-versus-host disease following in utero transplantation of S-59 psoralen/ultraviolet a light-treated, sensitized T cells and adult T cell-depleted bone marrow in fetal mice J Immunol 169 2002 6133 6140
87. G.S. Wengler, A. Lanfranchi, T. Frusca, R. Verardi, A. Neva, and D. Brugnoni In-utero transplantation of parental CD34 haematopoietic progenitor cells in a patient with X-linked severe combined immunodeficiency (SCIDXI) Lancet 348 1996 1484 1487
88. R.H. Buckley, S.E. Schiff, R.I. Schiff, L. Markert, L.W. Williams, and J.L. Roberts Hematopoietic stem-cell transplantation for the treatment of severe combined immunodeficiency N Engl J Med 340 1999 508 516
89. M.O. Muench, J. Rae, A. Barcena, T. Leemhuis, J. Farrell, and L. Humeau Transplantation of a fetus with paternal Thy-1(+)CD34(+)cells for chronic granulomatous disease Bone Marrow Transplant 27 2001 355 364
90. M.J. Cowan, and M. Golbus In utero hematopoietic stem cell transplants for inherited diseases Am J Pediatr Hematol Oncol 16 1994 35 42
91. A.W. Flake, and E.D. Zanjani In utero hematopoietic stem cell transplantation: a status report JAMA 278 1997 932 937
92. F. Orlandi, A. Giambona, F. Messana, M. Marino, I. Abate, and R. Calzolari Evidence of induced non-tolerance in HLA-identical twins with hemoglobinopathy after in utero fetal transplantation Bone Marrow Transplant 18 1996 637 639
93. M. Westgren, O. Ringden, S. Eik-Nes, S. Ek, M. Anvret, and A.M. Brubakk Lack of evidence of permanent engraftment after in utero fetal stem cell transplantation in congenital hemoglobinopathies Transplantation 61 1996 1176 1179
94. S. Slavin, E. Naparstek, M. Ziegler, and A. Lewin Clinical application of intrauterine bone marrow transplantation for treatment of genetic diseases: feasibility studies Bone Marrow Transplant 9 Suppl 1 1992 189 190
95. D. Surbek, A. Schoeberlein, and A. Wagner Perinatal stem-cell and gene therapy for hemoglobinopathies Semin Fetal Neonatal Med 13 2008 282 290
96. J.L. Touraine, D. Raudrant, A. Rebaud, M.G. Roncarolo, S. Laplace, and L. Gebuhrer In utero transplantation of stem cells in humans: immunological aspects and clinical follow-up of patients Bone Marrow Transplant 9 Suppl 1 1992 121 126
97. A. Hayward, D. Ambruso, F. Battaglia, T. Donlon, K. Eddelman, and R. Giller Microchimerism and tolerance following intrauterine transplantation and transfusion for alpha-thalassemia-1 Fetal Diagn Ther 13 1998 8 14
98. B.J. Bambach, H.W. Moser, K. Blakemore, V.L. Corson, C.A. Griffin, and S.J. Noga Engraftment following in utero bone marrow transplantation for globoid cell leukodystrophy Bone Marrow Transplant 19 1997 399 402
99. J.L. Touraine, D. Raudrant, and S. Laplace Transplantation of hemopoietic cells from the fetal liver to treat patients with congenital diseases postnatally or prenatally Transplant Proc 29 1997 712 713
100. J.L. Touraine, D. Raudrant, F. Golfier, A. Rebaud, R. Sembeil, and M.G. Roncarolo Reappraisal of in utero stem cell transplantation based on long-term results Fetal Diagn Ther 19 2004 305 312
101. S. Ashizuka, W.H. Peranteau, S. Hayashi, and A.W. Flake Busulfan-conditioned bone marrow transplantation results in high-level allogeneic chimerism in mice made tolerant by in utero hematopoietic cell transplantation Exp Hematol 34 2006 359 368
102. M. Andreani, S. Nesci, G. Lucarelli, P. Tonucci, S. Rapa, and E. Angelucci Long-term survival of ex-thalassemic patients with persistent mixed chimerism after bone marrow transplantation Bone Marrow Transplant 25 2000 401 404
103. M.C. Walters, M. Patience, W. Leisenring, J.R. Eckman, J.P. Scott, and W.C. Mentzer Bone marrow transplantation for sickle cell disease [see comments] N Engl J Med 335 1996 369 376
104. A.W. Flake, and E.D. Zanjani Treatment of severe combined immunodeficiency N Engl J Med 341 1999 291 292
105. H. Bjorgvinsdottir, C. Ding, N. Pech, M.A. Gifford, L.L. Li, and M.C. Dinauer Retroviral-mediated gene transfer of gp91phox into bone marrow cells rescues defect in host defense against Aspergillus fumigatus in murine X-linked chronic granulomatous disease Blood 89 1997 41 48
106. D. Hollenbaugh, L.H. Wu, H.D. Ochs, S. Nonoyama, L.S. Grosmaire, and J.A. Ledbetter The random inactivation of the X chromosome carrying the defective gene responsible for X-linked hyper IgM syndrome (X-HIM) in female carriers of HIGM1 J Clin Invest 94 1994 616 622
107. T.R. Bauer Jr., Y.C. Gu, L.M. Tuschong, T. Burkholder, J.D. Bacher, and M.F. Starost Nonmyeloablative hematopoietic stem cell transplantation corrects the disease phenotype in the canine model of leukocyte adhesion deficiency Exp Hematol 33 2005 706 712
108. R.A. Sokolic, T.R. Bauer, Y.C. Gu, M. Hai, L.M. Tuschong, and T. Burkholder Nonmyeloablative conditioning with busulfan before matched littermate bone marrow transplantation results in reversal of the disease phenotype in canine leukocyte adhesion deficiency Biol Blood Marrow Transplant 11 2005 755 763
109. T.R. Bauer Jr., K.E. Creevy, Y.C. Gu, L.M. Tuschong, R.E. Donahue, and M.E. Metzger Very low levels of donor CD18+ neutrophils following allogeneic hematopoietic stem cell transplantation reverse the disease phenotype in canine leukocyte adhesion deficiency Blood 103 2004 3582 3589